Crowding induces differences in the diffusion of thermophilic and mesophilic proteins: A new look at neutron scattering results

Biophysical Journal

Volumn 101, Issue 11, 2011, Pages 2782-2789

  Marcos, Enrique ^a   Mestres, Pau ^a   Crehuet, Ramon ^a  

^a INSTITUTE OF ADVANCED CHEMISTRY OF CATALONIA IQAC CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

LACTATE DEHYDROGENASE; MALATE DEHYDROGENASE;

ANIMAL; ARTICLE; CHEMICAL STRUCTURE; COMPUTER SIMULATION; DIFFUSION; ENZYMOLOGY; MACROMOLECULE; METABOLISM; METHANOCOCCUS; NEUTRON DIFFRACTION; RABBIT; SMALL ANGLE SCATTERING; STATIC ELECTRICITY; TEMPERATURE;

ANIMALS; COMPUTER SIMULATION; DIFFUSION; L-LACTATE DEHYDROGENASE; MACROMOLECULAR SUBSTANCES; MALATE DEHYDROGENASE; METHANOCOCCUS; MODELS, MOLECULAR; NEUTRON DIFFRACTION; RABBITS; SCATTERING, SMALL ANGLE; STATIC ELECTRICITY; TEMPERATURE;

EID: 82955206478     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.09.033     Document Type: Article

References (67)

1. C. Vieille, and G.J. Zeikus Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability Microbiol. Mol. Biol. Rev. 65 2001 1 43
2. P. Závodszky, and J. Kardos G.A. Petsko Adjustment of conformational flexibility is a key event in the thermal adaptation of proteins Proc. Natl. Acad. Sci. USA 95 1998 7406 7411
3. G. Hernandez, and F.E. Jenney Jr. D.M. LeMaster Millisecond time scale conformational flexibility in a hyperthermophile protein at ambient temperature Proc. Natl. Acad. Sci. USA 97 2000 3166 3170
4. J. Fitter, and J. Heberle Structural equilibrium fluctuations in mesophilic and thermophilic alpha-amylase Biophys. J. 79 2000 1629 1636
5. M. Wolf-Watz, and V. Thai D. Kern Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair Nat. Struct. Mol. Biol. 11 2004 945 949
6. J.A. Butterwick, and J. Patrick Loria A.G. Palmer 3rd Multiple time scale backbone dynamics of homologous thermophilic and mesophilic ribonuclease HI enzymes J. Mol. Biol. 339 2004 855 871
7. L. Salmon, and G. Bouvignies M. Blackledge Nuclear magnetic resonance provides a quantitative description of protein conformational flexibility on physiologically important time scales Biochemistry 50 2011 2735 2747
8. M. Tehei, and D. Madern G. Zaccai Neutron scattering reveals the dynamic basis of protein adaptation to extreme temperature J. Biol. Chem. 280 2005 40974 40979
9. G. Zaccai How soft is a protein? A protein dynamics force constant measured by neutron scattering Science 288 2000 1604 1607
10. M. Tehei, and B. Franzetti G. Zaccai Adaptation to extreme environments: macromolecular dynamics in bacteria compared in vivo by neutron scattering EMBO Rep. 5 2004 66 70
11. M. Tehei, and D. Madern G. Zaccai Fast dynamics of halophilic malate dehydrogenase and BSA measured by neutron scattering under various solvent conditions influencing protein stability Proc. Natl. Acad. Sci. USA 98 2001 14356 14361
12. M. Tarek, and D.J. Tobias Environmental dependence of the dynamics of protein hydration water J. Am. Chem. Soc. 121 1999 9740 9741
13. M. Tarek, G.J. Martyna, and D.J. Tobias Amplitudes and frequencies of protein dynamics: analysis of discrepancies between neutron scattering and molecular dynamics simulations J. Am. Chem. Soc. 122 2000 10450 10451
14. M. Tarek, and D.J. Tobias The dynamics of protein hydration water: a quantitative comparison of molecular dynamics simulations and neutron-scattering experiments Biophys. J. 79 2000 3244 3257
15. K. Wood, and A. Frölich M. Weik Coincidence of dynamical transitions in a soluble protein and its hydration water: direct measurements by neutron scattering and MD simulations J. Am. Chem. Soc. 130 2008 4586 4587
16. K. Wood, and S. Grudinin G. Zaccai Dynamical heterogeneity of specific amino acids in bacteriorhodopsin J. Mol. Biol. 380 2008 581 591
17. K. Wood, and D.J. Tobias M. Weik The low-temperature inflection observed in neutron scattering measurements of proteins is due to methyl rotation: direct evidence using isotope labeling and molecular dynamics simulations J. Am. Chem. Soc. 132 2010 4990 4991
18. S.R. McGuffee, and A.H. Elcock Atomically detailed simulations of concentrated protein solutions: the effects of salt, pH, point mutations, and protein concentration in simulations of 1000-molecule systems J. Am. Chem. Soc. 128 2006 12098 12110
19. S.R. McGuffee, and A.H. Elcock Diffusion, crowding & protein stability in a dynamic molecular model of the bacterial cytoplasm PLOS Comput. Biol. 6 2010 e1000694
20. P. Mereghetti, R.R. Gabdoulline, and R.C. Wade Brownian dynamics simulation of protein solutions: structural and dynamical properties Biophys. J. 99 2010 3782 3791
21. F. Gabel, and D. Bicout G. Zaccai Protein dynamics studied by neutron scattering Q. Rev. Biophys. 35 2002 327 367
22. J. Pérez, J.M. Zanotti, and D. Durand Evolution of the internal dynamics of two globular proteins from dry powder to solution Biophys. J. 77 1999 454 469
23. J.A. Hayward, and J.L. Finney J.C. Smith Molecular dynamics decomposition of temperature-dependent elastic neutron scattering by a protein solution Biophys. J. 85 2003 679 685
24. F. Gabel Protein dynamics in solution and powder measured by incoherent elastic neutron scattering: the influence of Q-range and energy resolution Eur. Biophys. J. 34 2005 1 12
25. L. Meinhold, and D. Clement J.C. Smith Protein dynamics and stability: the distribution of atomic fluctuations in thermophilic and mesophilic dihydrofolate reductase derived using elastic incoherent neutron scattering Biophys. J. 94 2008 4812 4818
26. B.I. Lee, and C. Chang S.W. Suh Crystal structure of the MJ0490 gene product of the hyperthermophilic archaebacterium Methanococcus jannaschii, a novel member of the lactate/malate family of dehydrogenases J. Mol. Biol. 307 2001 1351 1362
27. C.R. Dunn, and H.M. Wilks J.J. Holbrook Design and synthesis of new enzymes based on the lactate dehydrogenase framework Philos. Trans. R. Soc. Lond. B Biol. Sci. 332 1991 177 184
28. B. Hess, and C. Kutzner E. Lindahl GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
29. J.A. Hayward, and J.C. Smith Temperature dependence of protein dynamics: computer simulation analysis of neutron scattering properties Biophys. J. 82 2002 1216 1225
30. T. Róg, and K. Murzyn G.R. Kneller nMoldyn: a program package for a neutron scattering oriented analysis of molecular dynamics simulations J. Comput. Chem. 24 2003 657 667
31. H.J.C. Berendsen, and J.P.M. Postma J.R. Haak Molecular dynamics with coupling to an external bath J. Chem. Phys. 81 1984 3684 3690
32. W.L. Jorgensen, D.S. Maxwell, and J. Tirado-Rives Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids J. Am. Chem. Soc. 118 1996 11225 11236
33. W.L. Jorgensen, and J. Chandrasekhar M.L. Klein Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79 1983 926 935
34. T. Darden, D. York, and L. Pedersen Particle mesh Ewald - an N·log(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
35. B. Hess, and H. Bekker J. Fraaije LINCS: A linear constraint solver for molecular simulations J. Comput. Chem. 18 1997 1463 1472
36. M.B. Hamaneh, L. Zhang, and M. Buck A direct coupling between global and internal motions in a single domain protein? MD Investigation of extreme scenarios Biophys. J. 101 2011 196 204
37. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38 27-28
38. N.A. Baker, and D. Sept J.A. McCammon Electrostatics of nanosystems: application to microtubules and the ribosome Proc. Natl. Acad. Sci. USA 98 2001 10037 10041
39. F. Fogolari, A. Brigo, and H. Molinari The Poisson-Boltzmann equation for biomolecular electrostatics: a tool for structural biology J. Mol. Recognit. 15 2002 377 392
40. L. Holm, and S. Kääriäinen A. Schenkel Searching protein structure databases with DaliLite v.3 Bioinformatics 24 2008 2780 2781
41. R.J. Ellis Macromolecular crowding: obvious but underappreciated Trends Biochem. Sci. 26 2001 597 604
42. S. Kumar, and R. Nussinov How do thermophilic proteins deal with heat? Cell. Mol. Life Sci. 58 2001 1216 1233
43. P.I.W. de Bakker, P.H. Hünenberger, and J.A. McCammon Molecular dynamics simulations of the hyperthermophilic protein sac7d from Sulfolobus acidocaldarius: contribution of salt bridges to thermostability J. Mol. Biol. 285 1999 1811 1830
44. A.S. Thomas, and A.H. Elcock Molecular simulations suggest protein salt bridges are uniquely suited to life at high temperatures J. Am. Chem. Soc. 126 2004 2208 2214
45. C. Danciulescu, R. Ladenstein, and L. Nilsson Dynamic arrangement of ion pairs and individual contributions to the thermal stability of the cofactor-binding domain of glutamate dehydrogenase from Thermotoga maritima Biochemistry 46 2007 8537 8549
46. J.M. Vinther, S.M. Kristensen, and J.J. Led Enhanced stability of a protein with increasing temperature J. Am. Chem. Soc. 133 2010 271 278
47. A. Karshikoff, and R. Ladenstein Ion pairs and the thermotolerance of proteins from hyperthermophiles: a "traffic rule" for hot roads Trends Biochem. Sci. 26 2001 550 556
48. T. Ando, and J. Skolnick Crowding and hydrodynamic interactions likely dominate in vivo macromolecular motion Proc. Natl. Acad. Sci. USA 107 2010 18457 18462
49. N.V. Nucci, M.S. Pometun, and A.J. Wand Site-resolved measurement of water-protein interactions by solution NMR Nat. Struct. Mol. Biol. 18 2011 245 249
50. B. Halle Protein hydration dynamics in solution: a critical survey Philos. Trans. R. Soc. Lond. B Biol. Sci. 359 2004 1207 1223 discussion 1223-1224, 1323-1328
51. K. Modig, and E. Liepinsh B. Halle Dynamics of protein and peptide hydration J. Am. Chem. Soc. 126 2004 102 114
52. M. Ahmad, and W. Gu V. Helms Adhesive water networks facilitate binding of protein interfaces Nat. Commun. 2 2011 261
53. B. Halle, and M. Davidovic Biomolecular hydration: from water dynamics to hydrodynamics Proc. Natl. Acad. Sci. USA 100 2003 12135 12140
54. S. Melchionna, R. Sinibaldi, and G. Briganti Explanation of the stability of thermophilic proteins based on unique micromorphology Biophys. J. 90 2006 4204 4212
55. F. Sterpone, and C. Bertonati S. Melchionna Key role of proximal water in regulating thermostable proteins J. Phys. Chem. B 113 2009 131 137
56. N. Meechai, A.M. Jamieson, and J. Blackwell Translational diffusion coefficients of bovine serum albumin in aqueous solution at high ionic strength J. Colloid Interface Sci. 218 1999 167 175
57. F. Roosen-Runge, and M. Hennig F. Schreiber Protein diffusion in crowded electrolyte solutions Biochim. Biophys. Acta 1804 2010 68 75
58. T.J. Dolinsky, and J.E. Nielsen N.A. Baker PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations Nucleic Acids Res. 32 Web Server issue 2004 W665 W667
59. H. Li, A.D. Robertson, and J.H. Jensen Very fast empirical prediction and rationalization of protein pK(a) values Proteins 61 2005 704 721
60. R.R. Gabdoulline, and R.C. Wade Effective charges for macromolecules in solvent J. Phys. Chem. 100 1996 3868 3878
61. R.R. Gabdoulline, and R.C. Wade Simulation of the diffusional association of barnase and barstar Biophys. J. 72 1997 1917 1929
62. J. García De La Torre, M.L. Huertas, and B. Carrasco Calculation of hydrodynamic properties of globular proteins from their atomic-level structure Biophys. J. 78 2000 719 730
63. K. Hinsen The molecular modeling toolkit: A new approach to molecular simulations J. Comput. Chem. 21 2000 79 85
64. W.M. Haynes CRC Handbook of Chemistry and Physics 91st Ed. 2010-2011 CRC Press Boca Raton, FL
65. D. Madern, and C. Ebel G. Zaccai Differences in the oligomeric states of the LDH-like L-MalDH from the hyperthermophilic archaea Methanococcus jannaschii and Archaeoglobus fulgidus Biochemistry 40 2001 10310 10316
66. O.D. Velev, E.W. Kaler, and A.M. Lenhoff Protein interactions in solution characterized by light and neutron scattering: comparison of lysozyme and chymotrypsinogen Biophys. J. 75 1998 2682 2697
67. D.I. Svergun, and S. Richard G. Zaccai Protein hydration in solution: experimental observation by x-ray and neutron scattering Proc. Natl. Acad. Sci. USA 95 1998 2267 2272